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1 Department of Radiology, Imaging Research Division, University of Pittsburgh,
300 Halket St., Ste. 4200, Pittsburgh, PA 15213.
2 Department of Medicine, Division of Pulmonary, Allergy and Critical Care
Medicine, University of Pittsburgh, Pittsburgh, PA 15213.
3 Departments of Medicine and Epidemiology and University of Pittsburgh Cancer
Institute, University of Pittsburgh, Pittsburgh, PA 15213.
Received November 18, 2003;
accepted after revision February 4, 2004.
Supported by a grant from the George H. Love Foundation.
Abstract
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MATERIALS AND METHODS. Twenty-four male and 19 female patients with emphysema underwent lung volume reduction surgery, pulmonary function testing, and repeated CT. The tracheal air column was segmented from axial images. The sagittal and coronal dimensions of the intrathoracic trachea were determined. Tracheal morphology was quantified using the tracheal (coronal and sagittal dimensions) and circularity indexes. The results were compared with pulmonary function test results.
RESULTS. Morphologic appearance of the intrathoracic trachea was consistent before and 3 months after surgery. The group means of the tracheal length, mean area, and volume were 78.60 mm (± 16.88 mm), 283.84 mm2 (± 61.47 mm2), and 22.59 cm3 (± 7.69 cm3), respectively, before surgery and 67.53 mm (± 15.78 mm), 309.12 mm2 (± 79.83 mm2), and 20.99 cm3 (± 7.27 cm3), respectively, after surgery (p < 0.05). Mean tracheal indexes were 0.85 (± 0.11) before surgery and 0.82 (± 0.04) after surgery (p < 0.01). Mean circularity indexes were 0.91 (± 0.03) before surgery and 0.90 (± 0.04) after surgery (p < 0.05). The size of the trachea was significantly correlated with lung volume before and after surgery (p < 0.05). The changes in tracheal features and changes in pulmonary function were not correlated (p > 0.05), except for tracheal area (p < 0.05).
CONCLUSION. Our data suggest that tracheal dimensions reflect the severity of emphysema as reflected by increased lung volumes. Tracheal features were poor predictors of changes in postsurgical pulmonary function parameters evaluated in this preliminary study.
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The etiologic and physiologic mechanisms responsible for the saber-sheath shape are uncertain. Continuous remodeling and fixation of the tracheal cartilaginous rings as a result of chronic coughing are mechanisms commonly suggested for the saber-sheath trachea [2, 6]. Greene [2] also hypothesized that
...the trapped gas volume of upper lobe obstructive lung disease greatly restricts the potential side-to-side dimensions of the paratracheal mediastinum, forcing the trachea to remodel itself into a saber-sheath configuration in some patients with COPD [chronic obstructive pulmonary disease].
Elevated intrathoracic pressure combined with anteroposterior thoracic cavity expansion has also been suggested as a mechanism for the saber-sheath trachea [2, 7]. A combination of these mechanisms has also been suggested [2].
To our knowledge, no reports have been published on the chronologic changes in tracheal morphology with the natural progression of disease or as a result of intervention. Studies regarding the causes or implications of tracheal morphology have generally been conducted at a single point in time. Repeated evaluation of tracheal morphology over time in healthy patients as well as in patients with lung disease before and after therapeutic intervention may provide valuable information regarding the mechanism and implications of tracheal morphology.
Our study was designed to evaluate tracheal morphology before and after lung volume reduction surgery. Pulmonary function testing and CT were performed before and 3 months after lung volume reduction surgery. The air column of the intrathoracic trachea was segmented in the CT images from the level of the lateral aspect of the right first rib to the carina. A series of morphologic parameters were calculated for the intrathoracic trachea depicted on each CT image and were analyzed using descriptive statistics.
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Pulmonary function studies were performed in a standard manner as previously described [9]. The pulmonary function tests were performed using body plethysmography (Vmax 229 AutoBox, SensorMedics). All studies were performed within 3 days of the CT examinations.
Intrathoracic Trachea
Identification of the intrathoracic trachea began with automatically
segmenting the tracheal air column using a pixel-value threshold, 2D and 3D
region labeling, and simple logic. The most superior aspect of the
intrathoracic trachea was manually defined from the segmented CT image as the
level of the lateral aspect of the right first rib
(Fig. 1A). This level is the
most superior region in which thoracic pressure would be reflected on the lung
and, consequently, on the trachea. Next, the carina was manually identified
where the fleshy median between the tracheal bifurcation existed
(Fig. 1B). The CT image located
30 mm superior to the carina was defined as the most inferior aspect of the
intrathoracic trachea in order to eliminate from the analysis morphology
changes resulting from proximity to the bifurcation of the trachea.
Segmentation and subsequent quantification of the intrathoracic trachea were
performed using routines written in-house with Interactive Data Language
software (Research Systems). The data for before and 3 months after lung
volume reduction surgery were analyzed sequentially in time.
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Tracheal Quantification
The ratio of coronal to sagittal dimensions of the air column was used to
quantify tracheal morphology in the axial plane and is termed the
"tracheal index"
[1]. The coronal and sagittal
dimensions were determined by manually selecting two pixels on the axial CT
images depicting the segmented trachea using a computer mouse; therefore, this
process was subjective. For each dimension, the two pixels were located at
opposing ends of the trachea. Coronal and sagittal dimensions were not
necessarily defined in the strict anatomic planes if the trachea was oblique
to the anatomic planes (Fig.
2A), which avoids a potential limitation of measurements performed
on posteroanterior and lateral chest radiographs. The tracheal area was
calculated as the product of the pixel area and the number of segmented pixels
depicting the trachea in each axial CT image. The tracheal volume was
calculated as the product of the CT image thickness and the sum of the
tracheal areas in the CT images depicting the intrathoracic trachea.
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An objective circularity index was computed to quantify the tracheal
morphology in the axial plane. The circularity index was defined as the area
of intersection between the trachea and a reference circle divided by the
total area of the trachea as:
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Data Analysis
The data set was evaluated in terms of the entire group by sex and by
morphology (i.e., saber-sheath). Patients with and without the saber-sheath
shape were identified in a prestudy interpretation by an experienced thoracic
radiologist. The tracheal features (i.e., sagittal dimension, coronal
dimension, circularity index, tracheal index, tracheal length, axial plane
area, and volume) and pulmonary function test parameters (i.e., forced
expiratory volume in 1 sec (FEV1), total lung capacity, residual
volume, and percentage of residual volume divided by total lung capacity) were
evaluated before and 3 months after lung volume reduction surgery using a
two-tailed, paired Student's t test and Pearson's correlation
coefficient. The average values across each subject's intrathoracic trachea of
sagittal dimension, coronal dimension, tracheal index, circularity index, and
axial plane area were reported, whereas length and volume were single values
per subject. The comparisons across sex and morphology were evaluated using a
two-tailed, two-sample t test (with equal and unequal variances as
appropriate). The number of patients with increasing or decreasing parameter
values after lung volume reduction surgery was evaluated using a binomial
proportion test. The term "area" in this study refers to the
measured area of the trachea in the axial plane.
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All patients showed an improvement in FEV1 (Table 1). Residual volume and percentage of residual volume divided by total lung capacity decreased in all patients, and total lung capacity decreased in 41 of the 43 patients.
The size of the trachea (i.e., length, mean area, and volume) was significantly, positively correlated (p < 0.05) with measures of lung volume (i.e., total lung capacity and residual volume) both before and 3 months after lung volume reduction surgery (Table 2). The tracheal size changes from before until after lung volume reduction surgery were not significantly correlated with changes in pulmonary function test parameters (p > 0.05), except for the negative correlations between changes in area and changes in both residual volume and residual volume divided by total lung capacity (p < 0.05). Tracheal and circularity indexes were not significantly correlated (p > 0.05) with pulmonary function test parameters, except for the positive correlation between the mean tracheal index and the percentage of residual volume divided by total lung capacity before lung volume reduction surgery.
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Tracheal and circularity indexes were significantly smaller (i.e., narrower) and tracheal dimensions were significantly larger for men than for women (p < 0.05) (Table 3). The values of FEV1, total lung capacity, and residual volume were also significantly larger for men than for women (p < 0.05). The tracheal features, except for the circularity index, changed significantly from before until 3 months after lung volume reduction surgery for the men (p < 0.05). Although the tracheal feature in women changed uniformly (increased or decreased) with the entire group, only the changes in mean sagittal dimension, length, and mean area were significantly different (p < 0.05).
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Ten patients were identified as having the saber-sheath shape, and their tracheal and circularity indexes were significantly smaller (i.e., narrower) and sagittal dimensions significantly larger than in patients without the saber-sheath shape (p < 0.05) (Table 4). Before lung volume reduction surgery, the percentage of residual volume divided by total lung capacity (the only pulmonary function test parameter), the mean area, and the volume were significantly different between the two groups (p < 0.05). Changes in the tracheal features for the saber-sheath group were similar to those for the entire group, but only length and volume changes were significant (p < 0.05). Tracheal and circularity indexes of the saber-sheath patients were significantly, positively correlated with total lung capacity and residual volume before lung volume reduction surgery (p < 0.05) (Table 5). Tracheal length was negatively correlated with FEV1 (p < 0.05) and was positively correlated with residual volume (p < 0.05) before lung volume reduction surgery. The saber-sheath patients had essentially no significant correlations between the tracheal features and pulmonary function test parameters the 3 months after lung volume reduction surgery or in the changes between before and after lung volume reduction surgery (p > 0.05).
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Patients for our study were not recruited on the basis of tracheal features, and, therefore, the tracheal features may be representative of the population of emphysema patients who are candidates for lung volume reduction surgery. The tracheal sagittal dimensions, coronal dimensions, and areas of the patients in this study were comparable to published values for healthy patients [2, 11–13]. However, our patients had smaller tracheal indexes than those reported for healthy patients [2, 7, 13].
In our study, the tracheal feature values were averaged across the CT images depicting intrathoracic trachea, which limits the ability to compare our study with studies that examined a single CT image. However, we also evaluated the minimum and maximum feature values across the intrathoracic trachea for all patients. These results were not substantially different from those reported for the average values and did not change the conclusions of our study. The tracheal index is commonly evaluated at 1 or 2 cm above the aortic arch [1, 2, 7, 11, 12]. However, the saber-sheath shape was observed to be consistent across the intrathoracic trachea in our study and in other reports [1, 4]. Vock et al. [13] observed a slight increase inferiorly in the tracheal index of healthy patients from 0.94 at the thoracic inlet to 1.00 halfway between the thoracic inlet and the carina (i.e., slightly superior to the aortic arch), and to 1.09 immediately above the carina.
Changes in the size of the trachea after lung volume reduction surgery in essence mimicked changes in lung volumes, revealing that the trachea is a somewhat adaptable structure. The length and volume of the trachea significantly decreased in 93% and 72% of the patients, respectively, and were strongly correlated to the pulmonary function test volume parameters (i.e., total lung capacity and residual volume) after lung volume reduction surgery (Tables 1 and 2). Additionally, tracheal area increased in 70% of the patients, possibly allowing greater airflow through the trachea, and was strongly correlated to FEV1 (Table 2). Our emphysema patients underwent lung volume reduction surgery to remove poorly functioning lung tissue and to relieve overinflation and thereby increase pulmonary function. The results were a decrease in total lung capacity, residual volume, and percentage of residual volume divided by total lung capacity accompanied by an increase in FEV1 after lung volume reduction surgery (Table 1).
A decrease in lung volume after lung volume reduction surgery is a likely mechanism for the changes in tracheal size without a dramatic change in axial plane morphology. This decrease in lung volume may have resulted in a change in pleural and transpulmonary pressures [9] and hence may alter the influence of those pressures on tracheal morphology. This huge increase in total lung capacity and residual volume as measured in these patients may force the anteroposterior thoracic cavity to expand [7] and may possibly compress and narrow the trachea [2, 7]. In addition, the elevated total lung capacity causes inferior depression of the diaphragm and potentially increases the length of the trachea. This inferior depression of the diaphragm has been observed to change to a more normal position after lung volume reduction surgery [14]. Therefore, decreasing lung volume and altering intrathoracic pressure may cause the trachea to shorten in the superoinferior direction and expand in the axial plane. However, if the tracheal cartilaginous rings have indeed remodeled and become fixated [2, 6], these changes may not be sufficient to allow the transtracheal pressure to dramatically alter the axial plane morphology of the trachea.
The results of this study indicate that tracheal features (i.e., morphology and size) do not predict changes in pulmonary function, as determined by the pulmonary function test parameters evaluated and, therefore, may not be relevant to the individual patient. The changes in tracheal features after lung volume reduction surgery were observed in most but not all patients for sagittal dimension, length, and volume (Table 1). Although pulmonary function showed statistically significant improvement after lung volume reduction surgery in all patients (Table 1), we do not have other measures, such as quality of life or exercise test results, to quantify the clinical effect on individual patients. Furthermore, no correlation was seen between the changes in the tracheal features and changes in the pulmonary function test parameters (Table 2).
The presence of the saber-sheath shape was also not a predictor of pulmonary function. Somewhat similarly, Trigaux et al. [7] concluded that the saber-sheath shape was the result of overinflation of the lung and was not correlated with airflow obstruction (i.e., FEV1) or parenchyma dysfunction. However, Greene and Lechner [1] suggested an association between the tracheal morphology and pulmonary function test parameters. Greene [2] further suggested that tracheal morphology correlated with clinical indexes of chronic obstructive pulmonary disease. The patients with saber-sheath trachea in our study had similar sagittal dimensions and areas but larger tracheal indexes and smaller coronal dimensions than did patients in the other studies [1, 2, 7]. In contrast to our study, Greene [2] reported a smaller tracheal area in patients with a saber-sheath trachea than in patients without it.
The thick slices of our images may have limited the accuracy of the measurement of tracheal dimensions because of the orientation of the trachea relative to the image plane [7] and partial volume averaging. The steep pixel value gradient between the air column and the tracheal wall should minimize the effects of slice thickness and volume averaging. Future studies using thinner image slices should also attenuate these effects. Because respiration was not externally suspended during the CT examination (e.g., spirometrically gated CT acquisition [15]), tracheal wall constriction and posterior membrane invagination during respiration were possible but probably extremely limited [6]. Additionally, it is uncertain if 3 months after surgery is sufficient time for a complete change of the trachea.
In conclusion, tracheal features (i.e., size and morphology) changed significantly after lung volume reduction surgery in most but not all of the patients in this study. The size of the trachea correlated to lung volumes before and after lung volume reduction surgery. These data suggest that elevated lung volumes with the consequent reconfiguration of the lungs and thoracic cavity play a role in determining tracheal dimensions in patients with severe chronic obstructive pulmonary disease and emphysema. We speculate that lateral compression of the trachea may play a role in tracheal dimensions. The only tracheal feature correlated with changes in pulmonary function test parameters before and after lung volume reduction surgery was tracheal area, with changes in residual volume and residual volume divided by total lung capacity. Therefore, tracheal features were poor predictors of changes in the pulmonary function test parameters evaluated in this preliminary study after lung volume reduction surgery. Perhaps the magnitude of the change after lung volume reduction surgery may have been insufficient to effect major changes in the tracheal features relative to pulmonary function test parameter changes. Additionally, other mechanisms may influence the trachea, such as pathologic changes in the trachea that may not be completely reversible.
Acknowledgments
We thank Amy Klym and Jill King from the University of Pittsburgh for their
dedicated assistance with data analysis and management.
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